Functional Ecology 2008, 22, 691– 698
doi: 10.1111/j.1365-2435.2008.01397.x
Persistent effects of maternal parasitic infection on
offspring fitness: implications for adaptive reproductive
strategies when parasitized
Blackwell Publishing Ltd
L. E. Schwanz*
Department of Biology, University of New Mexico, Albuquerque, NM 87131, USA
Summary
1. Maternal effects on offspring phenotype may represent adaptive strategies to optimize maternal
or offspring fitness given the maternal environment. The effect of maternal parasitic infection on
offspring phenotype has been largely ignored, despite the potential for such effects to be components of a maternal reproductive strategy. In addition, the persistence and fitness consequences
of maternal effects are understudied, particularly with respect to research on maternal parasitic
infection.
2. Deer mice (Peromyscus maniculatus) increase reproductive output by weaning heavier offspring
when infected with a schistosome parasite (Schistosomatium douthitti). Here, I examine the persistence
of maternal effects on offspring phenotype and evaluate potential consequences of maternal
parasitic infection for offspring lifetime fitness.
3. Offspring of parasitized females are born heavier, and this mass advantage persists in sons until
adulthood. Because adult body mass is known to influence adult reproductive success in deer mice,
parasitized mothers would have produced sons of higher reproductive success.
4. Neither maternal infection nor offspring mass influenced adult son aggression. Survival was
enhanced for heavier offspring post-weaning.
5. The production of heavier offspring by parasitized females, therefore, led to increased offspring
fitness through enhanced survival and potentially reproductive success. The resultant increase in
current maternal reproductive success in response to possible infection-induced decreases in future
reproductive opportunities supports the hypothesis that infected females trade-off between current
and future reproduction.
Key-words: fecundity compensation, phenotypic plasticity, rodent, terminal investment,
trematode
Introduction
Maternal effects describe changes to offspring phenotype due
to non-genetic maternal attributes (e.g. diet, propagule size),
and can include impacts on offspring gender, development,
size, behaviour, and viability (Roach & Wulff 1987; Deeming
& Ferguson 1991; Mousseau & Dingle 1991; Bernardo 1996;
Mousseau & Fox 1998a). Maternal effects are important for
population ecology because they can impact offspring lifehistories and population demography (Räsänen & Kruuk
2007). The translation of maternal phenotype or environment
to offspring phenotype may be associated with costs and
constraints and may be non-adaptive (e.g. Clark & Galef
*Correspondence author. E-mail: [email protected]
1995; Uller 2003; Uller et al. 2004). However, it may also be
an adaptive component of maternal reproduction (Mousseau
& Fox 1998b; Marshall & Uller 2007). For example, females
of poor condition may provide each offspring with less
provision, producing offspring of reduced size or viability
while maximizing maternal fitness (e.g. Shine & Downes
1999; McAdam & Boutin 2003; Gagliano & McCormick
2006). Alternatively, maternal effects may maximize offspring
and maternal fitness by matching offspring phenotype to
maternal or environmental conditions (Charnov 1982;
Sorci & Clobert 1995; Heeb et al. 1998; Shine & Downes 1999;
Kristan 2002, 2004). In order to understand the significance
of maternal effects, the persistence of these effects and
their fitness consequences for mothers and offspring must be
determined.
© 2008 The Author. Journal compilation © 2008 British Ecological Society
692
L. E. Schwanz
Variation in maternal condition frequently leads to variation in offspring size, sex, behaviour, or performance (e.g.
Hewison & Gaillard 1999; Shine & Downes 1999; McAdam
& Boutin 2003; Gagliano & McCormick 2006). An emerging
area of research into condition-dependent reproductive strategies examines the ways in which parasitic infection and
immunocompetence influence reproductive patterns (Forbes
1993; Sheldon & Verhulst 1996; Richner 1998; Agnew, Koella
& Michalakis 2000; Zuk & Stoehr 2002; Stoehr & Kokko
2006). Parasites are known to have extensive direct impacts
on host phenotypes, including physiology, behaviour and lifehistory (e.g. Schall, Bennett & Putnem 1982; Holmes & Zohar
1990; Kristan 2002; Schwanz 2006a; Lehmer et al. 2007;
Schwanz 2008). However, the indirect effects of parasites on
offspring phenotype (i.e. maternal effects) have been poorly
studied, despite their potential to be important components
of an adaptive host response (Sorci & Clobert 1995; Heeb
et al. 1998; Kristan 2002, 2004; Poulin & Thomas 2008).
In the deer mouse (Peromyscus maniculatus), infection
with the blood fluke Schistosomatium douthitti (Trematoda)
is chronic and leads to reduced liver function and altered
thermoregulation (Schwanz 2006a, 2008). In addition,
exposure to high doses of the parasite reduces host survival.
In response to parasitism, female deer mice alter their reproductive investment, producing heavier offspring at weaning,
although an equal number of offspring per litter (Schwanz
2008). An increase in reproductive investment in response to
a chronic infection that reduces survival may be a facultative reproductive strategy of infected females to compensate
for reduced future reproductive opportunities (i.e. terminal
investment or fecundity compensation, Minchella & LoVerde
1981; Clutton-Brock 1984; Schwanz 2006b). Under this
hypothesis, increased investment in current reproduction
must lead to an increase in current reproductive success.
Therefore, for the deer mouse – S. douthitti system, producing
heavier offspring should increase the fitness of offspring, thus
increasing current maternal reproductive success, presumably
at the expense of maternal survival or future reproduction
(Millar, Derrickson & Sharpe 1992; Millar 1994; Schwanz
2008). It is important to note that S. douthitti is an indirect
parasite, requiring an intermediate host (freshwater snail)
to complete its life cycle (Price 1931; Malek 1977). Therefore, infected mice cannot pass infection to offspring and
any effects of maternal parasitism on offspring phenotype are
indirect.
Here, I examine potential adaptive explanations for maternal
effects in this system. Because infected females produce
heavier offspring, I first determine whether the increased
investment in offspring occurs during gestation or during
lactation in order to gain insight into the nature of the maternal
effect. I then explore how offspring mass influences offspring
fitness by examining: (i) how mass affects survival throughout
the life-history stages of offspring; and (ii) whether mass
differences at weaning are maintained until adulthood. Adult
mass in deer mice is known to influence female fecundity
and male territoriality and fertility, so maternal effects on
offspring adult mass would influence offspring reproductive
success (Fairbairn 1977, 1978; Dewsbury 1979; Millar 1983;
Myers & Master 1983; Schwanz 2008). If production of offspring of a greater size is an adaptive reproductive strategy by
infected mothers to increase current reproductive success,
I predict that heavier offspring will have greater survival or
that they will remain heavier in adulthood, where this mass
advantage will translate to reproductive benefits. In addition,
I examine whether maternal parasitism has indirect effects on
offspring survival and behaviour independent of mass effects.
Finally, male aggression is examined and is predicted to increase
with body mass (Fairbairn 1978; Dewsbury 1979).
Methods
EXPERIMENTAL DESIGN
Adult deer mice (P. maniculatus rufinus) were 5th–9th generation
laboratory-reared animals from New Mexico (Botten, Ricci & Hjelle
2001). Mice were maintained in standard rodent cages on a 12 : 12
light:dark cycle and provided food (Formulab Diet 5008) and water
ad libitum (Schwanz 2006a, 2008). The experiment was initiated
with infection or sham-infection of females with S. douthitti. Details
on the parasite life cycle and the infection procedure can be found in
Schwanz (2006a, 2008). Briefly, the aquatic stage of the parasite
life cycle that is infective to rodents (cercaria) was collected from
patent snails (snails that are shedding parasites) under a dissecting
microscope and fed to the experimental mice. Use of a dissecting
microscope allowed approximate counts of the parasites fed to each
mouse. Fifty-one virgin, mature female mice (70–159 days old) were
divided into three treatments. Mice in the low dose (LD) treatment
(N = 20) received 30–50 parasites, those in the high dose (HD)
treatment (N = 10) received 100–150 parasites, and those in the
control treatment (N = 21) were sham-infected by providing
uncontaminated water to the mice.
At 30 days after infection (DAI), when eggs typically begin being
released from the host, females were randomly paired with uninfected,
mature males (100–346 days old). Pairs were housed together continuously for 150 days, during which time all breeding events were
recorded (see below). For pairs that bred, first litters were typically
born 30–60 days after pairing (c. 60–90 DAI), and post-partum estrus
was typical (Schwanz 2008). At 180 DAI, females were euthanized
with CO2 and dissected to confirm infection status via examination
of liver homogenate for S. douthitti eggs or larvae (see Schwanz 2006a).
Parasite load was not estimated. Final sample sizes of number of
offspring by female treatment were determined by confirmation of
maternal treatment status and the rate of reproduction of pairs
(12 control, 11 LD and 3 HD females produced at least one litter;
Schwanz 2008).
OFFSPRING GROWTH MEASUREMENTS
The experiment was conducted in 2004 (control and LD treatments)
and 2005 (all treatments). Maternal mass was measured weekly
following pairing. Cages were checked daily (for pregnant females,
based on weekly mass gain) or every other day (for other females) for
the presence of new litters. In 2005 only, offspring and parental mass
were recorded on the day of birth and every three days thereafter
until weaning (20–22 days after birth, normal age of independence,
Millar & Innes 1983; Millar & Threadgill 1987). During lactation,
offspring were individually-marked with unique numbers of bands
© 2008 The Author. Journal compilation © 2008 British Ecological Society, Functional Ecology, 22, 691–698
Maternal effects of parasitic infection 693
on their tails, drawn with a marker. This marking only persisted
following day 3, so individual identity was established from day 3.
At weaning for both years of study, offspring were given numbered,
metal ear tags (National Band and Tag Company, Newport, KY,
model 1005–1), and their mass and sex was recorded. Offspring were
then removed from the natal cage and maintained in a cage until
45-days-old in one of two ways: (i) with only littermates (Isolated),
or (ii) with a mixture of littermate and non-littermate offspring
within ±2 days of age (Mixed). Cages contained both sexes and
two to six offspring. The mixed caging was intended to more-closely
resemble natural competitive environments that offspring would
encounter in the wild. During this time, isolated and mixed cages
were not provided with rodent chow, but were given scattered,
mixed seed that was limited in quantity. One to two handfuls of
seed were provided every other day, depending on the number of
offspring per cage, and whether leftover seed was visible in the cage.
This amount of food was, therefore, a variable percentage of each
mouse’s daily requirement. Offspring grew during this stage (see
results), suggesting that the diet did not represent a substantial
dietary restriction. Because offspring of the different treatments
were mixed together in cages, the variability of the seed diet was
unlikely to introduce artificial treatment effects.
At day 45 (43–47 days), the typical age of sexual maturation
(Millar & Threadgill 1987), offspring body mass was recorded
again. A subset of offspring was maintained and weighed at day 90
(85–97 days), when body mass plateaus for deer mice (Linzey 1970;
Millar 1983). Between 45 and 90 days, male mice were housed alone
or with male littermates to minimize agonistic interactions. Females
were housed with other female littermates or non-littermates (up to
six mice per cage). Daily growth rates were calculated for each
offspring for three stages: (i) lactation (day 3–day 21), (ii) juvenile
(day 21–day 45), and (iii) adult (day 45–day 90). Daily growth values
were calculated as (mass at the end of the period – mass at the beginning
of the period)/(days between two measurements).
BEHAVIOUR TRIALS
Agonistic behaviour trials were performed in the dark during the
active phase of the deer mouse daily cycle (21:00–24:00 h). Each
trial paired a son of a control female and a son of an infected female
(LD only; all males were adults, ≥ 90 days old). Males were weighed
prior to the trial and marked on their tail with a black pen for visual
identification. Males were then placed into a circular arena (c. 19-L
bucket, 28-cm diameter) on separate sides of an opaque partition.
Following a 5-min acclimatization period, the partition was removed
and the arena was recorded for 20 min using the Nightshot Plus
feature on a Sony camcorder (CCD-TRV328 Hi8 NTSC Handycam,
Sony Electronics Inc.). No humans were present during the trial.
Each male was used only once in a behaviour trial. Tail markings and
side of acclimatization were randomized with respect to maternal
treatment.
Recordings of trials were scored for standard deer mouse
behaviours, including acts of aggression (wrestling on top, lunging,
boxing, rearing) and submission (wrestling on bottom, retreat;
Eisenberg 1968). Dominance scores were calculated for each
mouse as the proportion of scored behaviours that were aggressive
(lunging) rather than submissive (retreating from boxes or lunges).
Dominance in each trial was decided separately for (i) dominance
scores (dominant mouse had at least twice the dominance score) and
(ii) wrestling bouts (dominant mouse was on top during a wrestle
for at least twice as many wrestling bouts as the submissive mouse).
A mouse was declared as the winner of the trial if he was more
dominant in both dominance measures, or if he had higher dominance
according to one measure while the other measure was unclear or
provided insufficient data.
DATA ANALYSIS
Previous analysis of the reproductive data from this experiment
(Schwanz 2008) indicated that the two infection treatments (LD and
HD) did not differ significantly from each other in reproductive
variables (litter size, offspring size at weaning, etc), so they are combined here for statistical analysis into a single ‘infected’ treatment
group. Because few mice reared more than four litters and for the
sake of clear comparison to previous analyses (Schwanz 2008),
only offspring from the first four litters (parities) were included in
statistical analysis. Offspring mass during lactation (days 3–21) and
the juvenile stage (days 45–90) were analysed for treatment effects
using a repeated measures, nested  with parental pair of each
offspring as a factor nested within treatment. Offspring identity,
nested within parental pair and treatment, was entered in the models
as a random effect to account for repeated measures across individual
offspring. Offspring mass at day 0 and offspring growth rates were
examined for treatment differences with a nested . One control litter (three offspring) was excluded from all lactation analyses
because the offspring were not weighed during lactation. Other
predictors entered into the  models included sex (factor), litter
size (covariate), maternal parity (order of litter; factor), offspring age
(covariate), caging (isolated or mixed; factor), parity × treatment,
sex × treatment and age × treatment. Because sex was unknown at
birth and individual identity was not established until day 3, sex was
not available as a predictor of birth mass. Predictors (other than
treatment) with P > 0·15 were unlikely to provide any predictive
ability and were removed from the model.
Survival during lactation was assessed using only 2005 data
because litter sizes at birth are uncertain for 2004. A χ2-test was used
to analyse maternal treatment effects on survival mice from day 0 to
weaning. Logistic regression was used to test for effects of maternal
treatment and offspring body mass (mass at the beginning of the
time interval) on survival during the following intervals: days 3–21,
21– 45 and 45–90. For post-weaning intervals, offspring caging and sex
were included as predictors. Parental pair, nested within treatment,
was included in logistic models to account for parental effects.
For behaviour trials, competitiveness of sons from mothers of the
different treatments was examined using χ2-analyses. Percent mass
difference of ‘infected’ sons and ‘control’ sons [100 × (mass of ‘infected’
son – mass of ‘control’ son)/mass of lighter son] was also used as a
predictor of the likelihood of an ‘infected’ son winning a trial
(logistic regression). All statistics were performed with  version
6·0. Significance was assessed at P = 0·05, while 0·05 < P < 0·10 was
considered as statistical trend.
Results
MASS
At birth, offspring from infected mothers were significantly
heavier than offspring of control mothers, and mass was
negatively correlated with litter size (Nested , with birth
litter size: treatment P = 0·004, pair (treatment) P < 0·0001,
birth litter size P < 0·0001; or with weaned litter size: treatment
P < 0·0001, pair (treatment) P < 0·0001, litter size P < 0·0001;
Nobs = 103). Mass during lactation (days 3–21) remained
© 2008 The Author. Journal compilation © 2008 British Ecological Society, Functional Ecology, 22, 691– 698
694
L. E. Schwanz
Fig. 1. Average body mass during lactation of male and female
offspring from control and infected mothers (days 3–21, averaged across
all parities). Sample sizes are as follows: ‘infected’ sons (35), ‘infected’
daughters (30), ‘control’ sons (18), and ‘control’ daughters (25).
significantly greater for offspring of infected females
compared to those of uninfected females (Fig. 1, Table 1).
Offspring sex did not influence offspring mass during lactation, but parity had a significant effect (LS means ± SE,
parity 1: 6·8 ± 0·1; parity 2: 5·9 ± 0·1; parity 3: 6·0 ± 0·2;
parity 4: 6·4 ± 0·2).
Individual offspring mass at sexual maturity (45 days)
was correlated with mass at weaning (N = 240, r2 = 0·338,
Table 1. Nested, repeated measures  models reporting the
effect of predictors on mass of offspring during lactation (2005 only)
and in adulthood
Model
d.f.
d.f.
denom
F
P
Lactation mass, days 3–21 Nobs = 757
Maternal treatment
1
88·07
Pair (treatment)
12
88·09
Parity
3
89·08
Parity × Treatment
3
89·2
Litter size
1
87·63
Offspring age
1
648·2
Offspring age × Treatment
1
648·2
6·66
15·06
8·44
7·25
29·31
11 660
22·90
0·0115
< 0·0001
< 0·0001
0·0002
< 0·0001
< 0·0001
< 0·0001
Adult mass, days 45–90 Nobs = 370
Maternal treatment
1
Pair (treatment)
23
LS
1
Offspring age
1
Offspring age × Treatment
1
Sex
1
Sex × Treatment
1
3·19
2·74
17·76
203·27
3·43
29·03
3·82
0·0752
< 0·0001
< 0·0001
< 0·0001
0·0656
< 0·0001
0·0519
225·2
221
220·2
171·5
171·1
218·6
218·5
Offspring ID, nested in pair and treatment was entered as a random
effect to account for repeated measures. Caging was not used as
a predictor of mass during lactation because the caging effect was
only established after weaning. Predictors were removed from the
model if P > 0·15.
Fig. 2. Average body mass of male and female offspring from control
and infected mothers at sexual maturity (45 days) and asymptotic
adult mass (90 days). Error bars are 1 SD. Numbers above bars are
offspring sample sizes.
P < 0·0001). The mass of offspring at 90 days was correlated
with mass at maturity (N = 126, r2 = 0·321, P < 0·0001) and
at weaning (N = 127, r2 = 0·382, P < 0·0001). Females and
offspring from larger litters were at a size disadvantage in
adulthood (Table 1). Average adult mass of male and female
offspring combined did not differ significantly between maternal
treatments, although a statistical trend was apparent (Fig. 2,
Table 1). However, based on the nearly-significant sex × treatment
interaction, post hoc Tukey HSD tests were evaluated
(significance was assessed by  at α = 0·05) and revealed
that adult sons of infected females remained larger than sons
of control females (P < 0·05), but no treatment effects on the
mass of daughters persisted in adulthood (P > 0·05).
GROWTH
Growth from day 3 until weaning did not differ between
treatments (Table 2). Growth during lactation was negatively
related to litter size, varied according to parity (LS means ± SE,
parity 1: 0·51 ± 0·01; parity 2: 0·39 ± 0·01; parity 3: 0·39 ± 0·01;
parity 4: 0·43 ± 0·02), but was not related to offspring sex.
From weaning until sexual maturity, juvenile daily growth
rate was higher for males than females, but was not related to
maternal infection treatment (Table 2). Daily adult growth
rate (days 45–90) was greater for male offspring than female
offspring, but did not differ according to maternal treatment
(Table 2).
SURVIVAL
From day 0 to weaning, survival of offspring of control mothers
(66·2%, 43 of 65) and of infected mothers (61·3%, 65 or
106) did not differ significantly (χ2 = 0·41, P = 0·52). Most
mortality for control offspring occurred during the first
3 days (only four offspring died after day 3), whereas 28 of 41
© 2008 The Author. Journal compilation © 2008 British Ecological Society, Functional Ecology, 22, 691–698
Maternal effects of parasitic infection 695
Table 2. Results (P-values of predictors) of
nested  models examining daily
growth rates of offspring during lactation
(2005 only), juvenile and adult stages
Nobs
Npairs (control, infected)
Maternal treatment
Pair (treatment)
Sex
Sex × Treatment
Litter size
Parity
Parity × Treatment
Juvenile caging
Lactation
daily growth
rate, 3–21 days
Juvenile daily
growth rate,
21– 45 days
Adult daily
growth rate,
45–90 days
108
5, 9
0·170
< 0·0001
–
–
< 0·0001
< 0·0001
0·0002
NA
240
11, 14
0·229
< 0·0001
< 0·0001
0·031
–
–
–
–
127
11, 12
0·279
0·0002
0·009
–
0·082
–
–
–
Caging was not used as a predictor of lactation growth rate because the caging effect was only
established after weaning. Predictors were removed from the model if P > 0·15.
Table 3. Influence of predictors (P-values)
on offspring survival during lactation (2005
only), juvenile and adult intervals
Pair (treatment)
Maternal treatment
Offspring mass (direction of effect)
Sex [Female (F) vs. Male (M)]
Caging [Isolated (I) vs. Mixed (M)]
Lactation
survival,
days 3–21
Juvenile
survival,
days 21– 45
Adult
survival,
days 45–90
< 0·0001
0·995
0·780
–
–
0·481
0·998
0·022 (+)
0·941
0·094 (I > M)
0·013
0·995
0.265
0·014 (F < M)
0·039 (I > M)
Offspring mass at the beginning of each interval was used as the covariate. Caging and sex were
not entered as factors in the model of lactation survival because caging treatments had not been
established by weaning, and sex was not known for offspring that did not survive lactation.
offspring of infected mothers that did not survive until
weaning, died after day 3. Survival from day 3 until weaning
(when individual identity can be tracked) was not influenced
by maternal infection or offspring mass (Table 3).
Survival of offspring after weaning was high in the laboratory.
Only 7 of 249 offspring suffered mortality between days 21
and 45, and juvenile survival was positively influenced by
offspring mass at day 21 (Table 3). Of the 154 offspring
maintained from days 45 to 90, 26 died. Survival from
maturation until 90-days-old was not influenced by offspring
mass when offspring sex was taken into account. Adult survival was reduced for offspring that were housed in mixed
cages during the juvenile phase.
BEHAVIOUR TRIALS
In 22 of 26 behaviour trials, winners could be assigned. Three
of the remaining trials yielded insufficient behavioural
data, while one trial had conflicting results from wrestling
and dominance scores and was declared undecided. Sons of
parasitized mothers were not more or less likely to win a trial
when considering all trials (14 of 22 won, χ2 = 1·59, P = 0·21)
or only trials with a percent mass difference of ≤ 10% (7 of 10
won, χ2 = 1·51, P = 0·22). Lighter males won 73% of fights,
but effects of offspring mass on outcome of fights was not significant (N = 22, P = 0·07; Fig. 3).
Fig. 3. Wins (= 1) and losses (= 0) of behavioural trials by sons of infected
females when paired with sons of control females. The percent mass
difference between males in each trial was calculated as [100 × (‘infected’
son’s mass – ‘control’ son’s mass)/lighter male’s mass].
Discussion
Maternal effects are widespread in animals and may represent
adaptive strategies to increase maternal fitness (Mousseau
& Fox 1998b; Marshall & Uller 2007). Effects of maternal
parasitic infection on offspring phenotype may have
© 2008 The Author. Journal compilation © 2008 British Ecological Society, Functional Ecology, 22, 691– 698
696
L. E. Schwanz
consequences for offspring and maternal fitness and may
be part of an adaptive plastic response by parasitized females
to ameliorate the fitness costs of parasitism. Despite this potential importance for maternal effects in disease ecology, we
know little about the persistence of these maternal effects, or
the consequences for multiple components of offspring
and maternal fitness (Sorci & Clobert 1995; Heeb et al.
1998; Kristan 2002, 2004; Poulin & Thomas 2008).
INDIRECT EFFECTS OF PARASITIC INFECTION
In the deer mouse, maternal parasitic infection with S. douthitti
had lasting effects on offspring mass. Infected mothers birthed
and weaned offspring of greater mass, and produced larger
adult sons. The persistence of mass effects was reflected by
equivalent daily growth rates. Smaller offspring did not show
compensatory growth following weaning, as is often observed
in rodents (Sikes 1998; Oksanen, Koskela & Mappes 2002).
Only two previous studies in rodents have demonstrated a
positive effect of maternal infection on offspring size (Kristan
2002, 2004).
Producing offspring of greater mass had many fitness
benefits for the offspring through improved reproductive
success and survival. In deer mice, greater mass in females
often leads to greater fecundity (Millar 1983; Myers & Master
1983). Heavier adult male Peromyscus are more likely to
win agonistic encounters and appear to have an advantage
in maintaining territories (Fairbairn 1977, 1978; Dewsbury
1979). During this experiment, female fecundity was positively
related to maternal mass at parturition (Schwanz 2008),
but daughters of infected females did not remain larger as
adults to gain the reproductive benefits of greater adult mass.
Although this study found no evidence that larger mass
benefited males in agonistic trials, the persistent mass
advantage of sons of infected females in adulthood may still
indicate that being born heavier provides improved reproductive success of sons.
Larger offspring also had enhanced survival as juveniles.
Although post-weaning survival for deer mice in the field is
typically high (c. 0·8 survival for 2 weeks, Millar & Innes
1983), it is lower than the survival recorded in this laboratorybased study, raising questions as to whether this study provides an adequate test of post-weaning survival. Large body
mass may be more important for offspring survival in natural
settings than in the laboratory, suggesting that the results
recorded in this laboratory study may be enhanced and pertinent for wild mouse populations. Because offspring lifetime
fitness is determined by survival and reproductive success, this
study demonstrates that the production of larger offspring
by infected mothers clearly enhances multiple components of
offspring lifetime fitness.
Additional indirect effects of maternal parasitic infection
were limited. Although research in mammals has demonstrated effects of maternal condition on a son’s aggression
(Meikle & Westberg 2001), maternal infection status here had
no effect on the dominance of sons. In addition, survival was
not influenced by maternal infection. However, the analysis
of lactation survival combining offspring mass and maternal
treatment could only assess survival from day 3. Therefore, it
may not provide an adequate test of the importance of
these factors for survival during lactation due to the disparity
between treatments in the timing of offspring mortality
(largely before day 3 for control offspring). Additional effects
of maternal infection have been recorded in laboratory mice,
where offspring of mothers infected with nematodes are more
likely to recover from direct infection (Kristan 2002, 2004).
Schistosome resistance as a maternal effect in deer mice
was not examined here, and is an interesting future avenue of
research.
PERSISTENCE OF MATERNAL EFFECTS
Maternal effects on offspring phenotype were persistent in
this study of deer mice. In addition to effects of treatment on
offspring mass and resultant survival, litter size and parental
identity had persistent effects on offspring phenotype. Litter
size had a strong, negative effect on offspring mass that
persisted through the asymptotic mass of offspring. Because
maternal mass was positively correlated with litter size in this
experiment (Schwanz 2008), females of higher mass produced
larger litters with offspring that remained small in body
mass throughout their lives, producing a negative association
between maternal and offspring mass (Millar 1983). Whereas
maternal effects are often demonstrated at a single stage
(typically early) in offspring life or for a single performance
measure, the persistence of maternal effects and their consequences for multiple components of fitness often remain
unexamined (Fox & Savalli 1998; Kerr et al. 2007; Marshall &
Uller 2007). The results from this study demonstrate that
maternal effects can be quite persistent and have a strong
impact on offspring lifetime fitness (Clark & Galef 1995; Kerr
et al. 2007).
INFECTION AND MATERNAL REPRODUCTIVE
STRATEGIES
While it is clear that the production of heavier offspring
benefits offspring fitness, the fitness consequences for mothers
of producing larger offspring remain less clear. Producing
heavier offspring with higher fitness increases a mother’s
current reproductive success (anticipatory maternal effects,
Marshall & Uller 2007). In this respect, maternal effects in the
deer mouse – S. douthitti system appear to be part of an adaptive
maternal strategy to increase current reproductive success
when faced with decreased residual reproductive value
caused by infection (Schwanz 2008). Therefore, the response
of female deer mice to S. douthitti infection supports
hypotheses of adaptive host plasticity in life-history (i.e.
fecundity compensation and terminal investment hypotheses,
Minchella & LoVerde 1981; Clutton-Brock 1984; Forbes 1993;
Schwanz 2006b).
Some insight into maternal reproductive strategies may be
gained from considering the nature of the maternal effects.
That offspring of infected mothers were larger at birth suggests
© 2008 The Author. Journal compilation © 2008 British Ecological Society, Functional Ecology, 22, 691–698
Maternal effects of parasitic infection 697
that there are benefits during lactation that were not demonstrated here (e.g. in lactation survival). The persistence of a
mass difference to weaning suggests that post-weaning effects
of offspring mass are also important aspects of maternal
reproduction. This is because energetic investment in offspring
by deer mice increases dramatically during lactation and is
greater for heavier litters (Stebbins 1977; Millar & Innes 1983;
L.E. Schwanz, unpublished data), indicating that parasitized
females could have reduced energetic demands by reducing
milk production and weaning offspring of equivalent size as
those of control mothers. Greater reproductive competitiveness and juvenile survival in sons would be fitness benefits of
weaning heavier sons. Adult survival is a large determinant
of lifetime reproductive success in female deer mice (Millar
et al. 1992); however, the lack of a mass advantage in adult
daughters of infected mothers suggests that mothers do not
benefit from weaning larger daughters.
Parasitized females appear to have produced heavier weanings without an increase in energetic costs. This is because:
(i) energetic demands of gestation in laboratory deer mice are
minor compared to lactation and are not much higher than
non-breeding females (Stebbins 1977), and (ii) mothers in the
two treatments had equivalent investments during lactation
based on offspring growth rates and food consumption (infected
deer mice have equivalent food consumption and digestive
efficiencies as control mice, Schwanz 2006a, 2008). If larger
offspring have higher fitness and can be produced without
increased energetic demands, the ‘restraint’ in offspring birth
size shown by control deer mice suggests that birthing larger
offspring comes at a cost not apparent in laboratory settings.
For example, a larger litter mass may reduce maternal mobility
during pregnancy, impeding foraging or increasing predation risk (Brodie 1989; Lee et al. 1996; McLean & Speakman
2000; Shine 2003; Ghalambor, Reznick & Walker 2006).
Similarly, the birthing process itself may be riskier to embryo
or mother when the embryo is larger. Indeed, one infected
female died during parturition in this study. Production of
larger offspring at birth may also lead to reduced future
fecundity or survival of mothers. In order to confirm the
importance of larger offspring size for adaptive reproductive
investment by parasitized mothers, additional data are needed
on the impact on maternal survival of heavier offspring
during gestation, parturition and lactation.
Acknowledgements
Deer mice were obtained from B. Hjelle (UNM) via a Materials Transfer
Agreement. Snails and S. douthitti were kindly provided by D. Daniell (Butler
University). I thank D. Daniell, L. Hertel, E. S. Loker for materials and training
of parasitology techniques, and R. Ricci and F. Gurule for all animal care. H.
Lease, E. Schultz, D. Swenton, C. Tech, and R. Ricci assisted with data collection. I am grateful to H. Anderson and J. Brown for assistance in transcribing
behavioural data from video recordings. Advice and assistance on the design
and implementation of this study were provided by D. Daniell, A. KodricBrown, D. Kristan, L. Hertel, E. Loker, R. Ricci, and members of the KodricBrown and Loker laboratories. This manuscript was improved by comments
from Janzen laboratory members and two anonymous reviewers. Funding
was provided by a National Science Foundation Graduate Research Fellowship.
All animal procedures were approved by the Institutional Animal Care and Use
Committee at the University of New Mexico.
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Received 4 December 2007; accepted 11 February 2008
Handling Editor: Francisco Bozinovic
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